Androgens Support Male Acrobatic Courtship Behavior by Enhancing Muscle Speed and Easing the Severity of Its Tradeoff With Force

Androgens Support Male Acrobatic Courtship Behavior by Enhancing Muscle Speed and Easing the Severity of Its Tradeoff With Force
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DOI:
10.1210/en.2017-00599
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发表时间:
2017-11-01
期刊:
影响因子:
4.8
通讯作者:
Yancey, Julia
Yancey, Julia
中科院分区:
医学2区
文献类型:
--
作者:
Fuxjager, Matthew J.;Miles, Meredith C.;Yancey, Julia

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大脑中的类固醇激素作用调节着许多动物用于求偶和竞争的复杂的社会表现,但人们越来越认识到外周也可能是一个有效的类固醇调节复杂行为的场所。然而,这种“自下而上”的行为流出调节机制在很大程度上是不清楚的。为了研究这个问题,我们研究了雄激素是如何通过骨骼肌系统来调节一种叫做金领侏儒鸟的热带鸟类复杂的求爱杂技的。作为表演的一部分,雄鸟在背部上方拍打翅膀的速度至少比正常飞行时拍打翅膀的速度快2倍。这种行为被称为“滚-扣”,是通过反复激活肱骨牵张肌——肩胛骨尾肌(SH)来实现的,它产生的收缩-放松循环速度与其他类群的“超高速”肌肉相似。我们报道雄激素受体(AR)的内源性雄激素激活维持了这种肌肉异常快速的收缩动力学,使组织在振荡频率> 100hz下产生独特的翅膀运动。我们还表明,这些影响根植于依赖于ar的收缩速度的增加,这不会产生可检测到的力产生成本。因此,AR增强了求爱表现所必需的SH速度,同时避免了预期的与力量的权衡,否则可能对飞行产生负面影响。因此,外围增强现实不仅建立了肌肉系统来执行复杂的翅膀显示,而且在某种程度上平衡了肌肉对其他维持生命行为的功能需求。
Steroid hormone action in the brain regulates many animals' elaborate social displays used for courtship and competition, but it is increasingly recognized that the periphery may also be a site for potent steroidal modulation of complex behavior. However, the mechanisms of such "bottom-up" regulation of behavioral outflow are largely unclear. To study this problem, we examined how androgenic sex hormones act through the skeletal muscular system to mediate elaborate courtship acrobatics in a tropical bird called the golden-collared manakin. As part of their display, males snap their wings together above their backs at rates that are at least 2xfaster than the normal wing-beat frequency used for flight. This behavior, called the roll-snap, is actuated by repeatedly activating a humeral retractor muscle-the scapulohumeralis caudalis (SH)-which produces contraction-relaxation cycling speeds similar to the "superfast" muscles of other taxa. We report that endogenous androgenic activation of androgen receptor (AR) sustains this muscle's exceptionally rapid contractile kinetics, allowing the tissue to generate distinct wing movements at oscillation frequencies > 100 Hz. We also show that these effects are rooted in an AR-dependent increase to contractile velocity, which incurs no detectable cost to force generation. Thus, AR enhances SH speed necessary for courtship display performance while avoiding the expected tradeoff with strength that could otherwise negatively influence aspects of flight. Peripheral AR therefore not only sets up the muscular system to perform a complex wing display, but does so in a way that balances the functional requirements of this muscle for other life-sustaining behavior.